The tree species pool of Amazonian wetland forests

13 Pages·2017·12.2 MB·English

RESEARCHARTICLE
The tree species pool of Amazonian wetland
forests: Which species can assemble in
periodically waterlogged habitats?
BrunoGarciaLuize1,2☯*,Jose´LeonardoLimaMagalhães3‡,HelderQueiroz4‡,Maria
AparecidaLopes3‡,EduardoMartinsVenticinque5‡,EvlynMa´rciaLeãodeMoraesNovo6‡,
ThiagoSannaFreireSilva1,2☯
1 ProgramadePo´s-Graduac¸ãoemEcologiaeBiodiversidade,InstitutodeBiociências,Universidade
EstadualPaulista(UNESP),RioClaro,SãoPaulo,Brazil,2 EcosystemDynamicsObservatory,Departamento
a1111111111
deGeografia,InstitutodeGeociênciaseCiênciasExatas,UniversidadeEstadualPaulista(UNESP),Rio
a1111111111
Claro,SãoPaulo,Brazil,3 ProgramadePo´s-graduac¸ãoemEcologia,InstitutodeCiênciasBiolo´gicas,
a1111111111 UniversidadeFederaldoPara´/EmbrapaAmazoˆniaOriental,Guama´,Bele´m,Para´,Brazil,4 Institutode
a1111111111 DesenvolvimentoSustenta´velMamiraua´,Tefe´,Amazonas,Brazil,5 DepartamentodeEcologia,Universidade
a1111111111 FederaldoRioGrandedoNorte—UFRN,Natal,RioGrandedoNorte,Brazil,6 DivisãodeSensoriamento
Remoto,InstitutoNacionaldePesquisasEspaciais,SãoJose´dosCampos,SãoPaulo,Brazil
☯Theseauthorscontributedequallytothiswork.
‡Theseauthorsalsocontributedequallytothiswork.
*[email protected]
OPENACCESS
Citation:LuizeBG,MagalhãesJLL,QueirozH,
LopesMA,VenticinqueEM,LeãodeMoraesNovo Abstract
EM,etal.(2018)Thetreespeciespoolof
Amazonianwetlandforests:Whichspeciescan WedeterminedthefilteredtreespeciespoolofAmazonianwetlandforests,basedoncon-
assembleinperiodicallywaterloggedhabitats?
firmedoccurrencerecords,tobetterunderstandhowtreediversityinwetlandenvironments
PLoSONE13(5):e0198130.https://doi.org/
10.1371/journal.pone.0198130 comparestotreediversityintheentireAmazonregion.Thetreespeciespoolwasdeter-
minedusingdatafromtwomainsources:1)acompilationofpublishedtreespecieslists
Editor:Andre´sViña,MichiganStateUniversity,
UNITEDSTATES plusoneunpublishedlistofourown,derivedfromtreeplotinventoriesandfloristicsurveys;
2)queriesonbotanicalcollectionsthatincludeAmazonianflora,curatedbyherbariaand
Received:January29,2018
availablethroughtheSpeciesLinkdigitalbiodiversitydatabase.Weappliedtaxonomic
Accepted:May14,2018
nameresolutionanddeterminedsample-basedspeciesaccumulationcurvesforbothdata-
Published:May29,2018 sets,toestimatesamplingeffortandpredicttheexpectedspeciesrichnessusingChao’s
Copyright:©2018Luizeetal.Thisisanopen analyticalestimators.Wereportatotalof3615validtreespeciesoccurringinAmazonian
accessarticledistributedunderthetermsofthe wetlandforests.Aftersurveyingalmost70yearsofresearcheffortstoinventorythediversity
CreativeCommonsAttributionLicense,which
ofAmazonianwetlandtrees,wefoundthat74%theserecordswereregisteredinpublished
permitsunrestricteduse,distribution,and
reproductioninanymedium,providedtheoriginal specieslists(2688treespecies).Treespeciesrichnessestimatespredictedfromeithersin-
authorandsourcearecredited. gledatasetunderestimatedthetotalpooledspeciesrichnessrecordedasoccurringinAma-
DataAvailabilityStatement:Allrelevantdataare zonianwetlands,withonly41%ofthespeciessharedbybothdatasets.Thefilteredtree
withinthepaperanditsSupportingInformation speciespoolofAmazonianwetlandforestscomprises53%ofthe6727treespeciestaxo-
files.
nomicallyconfirmedfortheAmazoniantreefloratodate.Thislargeproportionislikelytobe
Funding:BGLacknowledgesgrant#2015/24554- theresultofsignificantspeciesinterchangeamongforesthabitatswithintheAmazonregion,
0,SãoPauloResearchFoundation(FAPESP). aswellasinsituspeciationprocessesduetostrongecologicalfiltering.Theprovidedtree
JLLMacknowledgesCAPES/PDSE#
speciespoolraisesthenumberoftreespeciespreviouslyreportedasoccurringinAmazo-
88881.135761/2016-01andCAPES/Fapespa
1530801.EMVandTSFSacknowledgeCNPq nianwetlandsbyafactorof3.2.
productivitygrants#308040/2017-1and#310144/
2015-9,respectively.Thisworkwassupportedby
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ThetreespeciespoolofAmazonianwetlands
researchgrantsMCT/CNPq/CT-INFRA/GEOMA# Introduction
550373/2010-1and#382728/2010-6andNSF
Knowledgeaboutthebiodiversityexpectedforlargerregions,knownastheregionalspecies
Dimensions/BiotaFAPESPgrant#2012/50260-6,
SãoPauloResearchFoundation(FAPESP).The pool[1],isimportantforinferringevolutionaryprocessesincommunityassembly[2].Empiri-
fundershadnoroleinstudydesign,datacollection calstudiesdeterminingthespeciespooloflargeregionsarecentralfordisentanglingthecross-
andanalysis,decisiontopublish,orpreparationof scaleprocessesthatshapebiodiversitypatterns[3]butidentifyingthespeciespoolofaregion
themanuscript.
isnotatrivialtask.Itrequirestheaccumulationofseveralbiodiversitysurveys,well-spaced
Competinginterests:Theauthorshavedeclared acrosstheregionandcoveringallpossiblehabitattypes.Theverydefinitionofspeciespoolas
thatnocompetinginterestsexist. “thesetofspeciesabletoassemblewithinalocalcommunity”[1,4,5]mustbeconsidered
beforeattemptingitsdetermination,asthespeciespoolmaybedefinedintermsofadelimited
geographicregion(i.e.unfilteredpool),orregardingaspecifichabitattype(i.e.filteredpool)
[1,5].
TheAmazonencompassesmorethanonethirdofallNeotropicalplantdiversity[6,7],dis-
tributedamongseveralhabitatswithhighlevelsofheterogeneity[8].Tworecentlypublished
checklistsoftheAmazonianflorareportoveralltreespeciesrichnessbetween6727[9]and11
676[10]validspeciesrecordedinherbaria,biodiversityrepositoriesand/orinventories,witha
predictedrichnessofc.a.16000treespecies[10,11,12]basedoninventoryobservations.The
starkdifferencebetweenchecklistscomesfromamorethoroughtaxonomicreviewperformed
by[9],butregardlessofsource,bothlistscanbeconsideredasapproximationsoftheregional
unfilteredtreespeciespooloftheAmazonregion,initsbroadestsense[13].
However,theAmazonregioncoversmorethan7millionsquarekilometers,spanning40˚
oflongitude,25˚oflatitude,andanelevationalgradientofc.a.6000m,andmostoftheseveral
Amazonianhabitatsremainpoorlysampled[11,14],stronglylimitingourknowledgeofthe
trueregionalspeciespool.ItisunreasonabletoexpectthatallAmazoniantreespeciesareable
tooccupyeveryenvironment,andthusbepartofthespeciespoolsofallhabitats.Thus,to
trulyunderstandtheprocessescontrollingtheassemblyandmaintenanceofAmazondiversity,
wemustimproveourknowledgeregardingthefilteredspeciespools[1]ofthediversehabitats
comprisingtheAmazonregion.
WetlandshavebeenextensivelypresentintheAmazonsinceatleasttheMiocene(30–23
Ma)[15,16],andPleistoceneoceanleveloscillations(2.5Ma)mayhavestronglyinfluenced
theirextentanddistributionovertime[17].Wetlandscurrentlycover8.4×105km2ofthe
Amazonlowlands(c.a.17%[18]),ofwhichapproximately70%arecoveredbyforests[19].
Totalextentmaybeevenhigher,comprisingupto30%oftheentireAmazonbasin,ifwecon-
siderhydromorphicsoilsalongsmallerstreams[20–22].MostAmazonianwetlandsshow
monomodalseasonalfluctuationsinwaterstageand/orwatertableheights,knownastheflood
pulse[20],whichhasbeeninferredtooccuratleastsincethePaleocene(66Ma)[23].
Hydrologicalseasonalityinfluencesedaphicconditions,leadingtohydrologicalsegregation
ofspeciesniches[24,25]asplantsdevelopthephysiologicalandecologicaladaptationsneces-
sarytosurviveseveralfloodsanddroughtsduringtheirlifespan[26–31].Thehydrological
regimeexperiencedbyeachindividualtreeoccurringintheAmazonianwetlandsdependson
localinteractionsbetweenbasinhydrologyandlocalgeomorphology[32],whichcreatestrong
gradientsoffloodheightandduration,shapingtreespeciesdiversificationandgeographical
distributionacrossscales[22,33–37].Wecanthusconsiderwetlandshabitatsasenvironmental
filters,selectingindividualsandspecieswhichcantoleraterecurrentinundationanddrought
duringtheirlifespan(e.g.:Hymatanthus [30];Inga[38]),anditisverylikelythatAmazonian
wetlandspecieshaveevolvedintoaparticularlyfilteredspeciespool.
WhilemosttreediversitystudiesintheAmazonstillfocusonuplandforests,therehasbeen
growinginterestinunderstandingtheinfluenceofwater-saturatedenvironmentsonquestions
relatedtotreerichness[21,37,39],compositionalpatterns[35,39,40],andphylogenetic
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ThetreespeciespoolofAmazonianwetlands
diversity[38,41,42].AvailabletreespecieslistsforAmazonianwetlandsplacetheeutrophic
floodplain(várzea)forestsastherichestwetlandforestsintheworld,with918confirmedtree
species[33],andarecentsurveyofBrazilianAmazonianwetlandsraisesthisnumberto1119
treespecies[22],comprising16%ofthe6727treespeciesreportedforoverallAmazonlow-
landforests[9].Furthermore,basedon542taxa(speciesandmorpho-species),threemainbio-
geographicregionsaresupportedbytreespeciescompositionalchangesalongtheBrazilian
Amazonrivermainstem[35].Itisthusclearthatweneedamorecomprehensiveknowledge
ofthefilteredspeciespoolabletocolonizethesehabitats,tobetterunderstandthehydrological
dimensionofnichesoccupiedbyAmazoniantreespecies[24,25]anditsroleintheassembly
andevolutionofAmazonrainforests.
Here,weprovidethemostcomprehensiveestimatetodateofthefilteredtreespeciespool
abletoassembleinAmazonianwetlands,combiningtreespeciesrecordsfromherbariadata-
basesandpublishedandunpublishedtreespeciessurveysfromdifferenttypesofAmazonian
wetlandforests.WealsodiscussthepossibleroleofwetlandsinmaintainingAmazontree
diversity,andofferapredictiontotheexpectednumberofspeciescomprisingthetotalfiltered
treespeciespoolthatcansurviveinwetlandenvironments,assessinghowitcomparestothe
knownAmazontreefloraandpredictedbasinwidediversity.Finally,wediscusscurrentlimi-
tationsandbestpracticesforincreasingourbiogeographicalknowledgeofthemosttreespe-
ciesrichanddiversewetlandforestsintheworld.
Materialsandmethods
Datasets
Ourfirstdatasetcomprisesareviewofpublishedtreespecieslists(TSL)fromtreeplotinvento-
riesand/orfloristicsurveysconductedinAmazonianwetlandforests(Fig1),complemented
byonepreviouslyunpublishedprimaryinventoryofourown(S1Table).ToconstructTSL,
weonlyconsideredstudiesthatreportedcompletespecieslists,foranyAmazonianwetland
type[20].
Ourseconddatasetwasbuiltbyqueryingbotanicalcollections(BC)madeinAmazonian
wetlandforests,curatedbyherbaria(Fig1,S2Table)andincludedintheSpeciesLinkdigital
biodiversitydatabase(http://www.splink.org.br).Wequerieddigitizedvoucherlabelsusing
thefollowingkeywords:“Alagada”; “Alagado”; “Alagável”; “Aluvial”; “Alluvial”;“Área Úmida”;
“Brejo”; “Chavascal”;“Flooded”;“Flood”;“Floodplain”; “Hidromórfico”; “Hydromorphic”;
“Igapó”; “Inundada”; “Inundável”; “Restinga”; “Tahuampa”; “Várzea”. Wethenmergedall
botanicalrecordsreturnedforeachkeywordandfilteredtheserecordstoincludeonlyAngio-
spermspeciesandonlyspecimenscollectedintheAmazoniasensu-latissimoregion,asdefined
by[43](Fig1).
Taxonomicstandardization
Validcanonicalnamesforspecieswereachievedbyperformingtaxonomicnameresolution
forbothspeciesdatasets,usingtheTaxonomicNameResolutionService—TNRSV.4.0online
platform[46].WesetTNRStoperformnameresolutionwithoutallowingpartialmatches,
andwithaminimummatchthreshold>0.85.Theauthoritysourcesconsultedwere,inorder
ofrelevance,TROPICOS(http://www.tropicos.org)andTHEPLANTLIST(http://theplantlist.org),
lastupdatedonAugust2015(fordetailssee:http://tnrs.iplantcollaborative.org).FortheTSL
dataset,afterperformingtaxonomicnameresolution,wefilteredtheresultingrecordsto
removefamiliesknowntocompriseonlynon-treelifeforms,andweassumedallremaining
recordsafterfilteringcorrespondedtotreespecies.ThefilteredrecordsfromBCdatasetwere
matchedtothemostrecentAmazontreeflorachecklist[9],retainingonlyspeciesnames
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ThetreespeciespoolofAmazonianwetlands
Fig1.LocationofpublishedspecieslistsandherbariarecordsreportingtreespeciesonAmazonianwetlandsforests.Thereddotsarethelocationoftree
specieslists(TSL)frombotanicalinventoriesonAmazonianwetlands,bluedotsarethevoucherspecimensfrombotanicalcollections(BC).TheAmazonia
sensu-latissimoregionisdefinedin[43],wetlandareaswereobtainedfrom[44],andtheclassificationofmajorAmazonianrivertypesisgivenby[45].
https://doi.org/10.1371/journal.pone.0198130.g001
confirmedbytaxonomicspecialistsasvalidspeciesnamesandhavingatreelifeform(i.e.lig-
neoustrunkreaching10cmDBH).
Richnessestimation
WeusedtheTSLandBCdatasetstobuildseparatespecies-by-sampling-unitincidencematri-
ces,aggregatingincidencebystudyforTSL,andbyyearofcollectionforBC.Weusedthe
resultingmatricestoassessthechronologicalorderofincidenceofeachrecordedspecies,
buildingacumulativespeciescollector’scurveusingthe‘vegan’package[47]andtoobtaining
therespectivesample-basedspeciesaccumulationcurvesforeachdataset[48].Wethenused
thesample-basedcurvestopredicttheexpectedspeciesrichnessifcollectioneffortsweredou-
bled.Theinferredandestimatedsample-basedaccumulationcurvesandpredictionsofspecies
richnesswerecalculatedusingrarefactionandextrapolationfunctionsforincidencedatapro-
videdby[48],usingthe‘iNEXT’package[49].AllanalyseswereperformedinR3.3.2.[50].
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ThetreespeciespoolofAmazonianwetlands
Resultsanddiscussion
DeterminingthefilteredspeciespoolofAmazonianwetlands
Intotal,wereviewed69studiesreportingtreespecieslistsforinventoriesconducedonAmazo-
nianwetlandforests(S1Table),ofwhich16(~20%)didnotincludeacompletelistofspeciesand
couldnotbeaddedtotheTSLdataset.Fromthe53studiesincludedinTSL,werecovered21446
recordscomprising2688validtreespeciesnames(S3Table).Fromthese,weestimatethat3380
(lower95%=3305,upper95%=3455)treespecieswouldberecordedforAmazonwetlandfor-
estsifsamplingeffortwasdoubled(Fig2A).Neitherthecollector’scurve,northeestimatedsam-
ple-basedspeciesaccumulationcurveshowedsignsofreachinganasymptote(Fig2A),evenafter
almost70yearsofinventoriesbeingconductedinAmazonianwetlandforests.
Weretrieved231119plantoccurrencerecordsfromtheSpeciesLinkdatabase.Afterfiltering
forAngiospermsintheAmazonregion,performingtaxonomicnameresolutionandmatching
againstthereferencetreespecieslists,weretained20902recordsfor2408validtreespecies
names(BCdataset—S2TableandS3Table),lowerthantheobservedorexpectednumberof
treespeciesobtainedfromtheTSLdataset.FortheBCdataset,wepredictedanexpectedrich-
nessof2938treespecies(lower95%=2867,upper95%=3009)toberecordedforAmazo-
nianwetlandforestsifcollectioneffortsweredoubled(Fig2B).
PoolingtogethertheTSLandBCdatasetsconfirmedatotalof3615validtreespecies,com-
prising42348recordsoftreesoccurringinAmazonianwetlandforests(S3Table),ahigher
richnessthantheexpecteddoubling-effortpredictionsfromeitherisolateddataset.Thetwo
datasetsshared1481(c.a.41%)treespecies,with1207(c.a.33%)onlyrecordedbyTSLand
927(c.a.26%)treespeciesonlyrecordedbyBC.
Scopeandlimitationsofthedeterminedtreespeciespool
ThedeterminedtreespeciespoolofAmazonianwetlandforestscomprises3615validspecies,
encompassingenvironmentalconditionsfoundbetweendiversewetlandtypes[20].Thisisthe
Fig2.Cumulativecollector’scurveandsample-basedspeciesaccumulationcurvefortreespeciesinAmazonianwetlands.(A)Treespecieslists(TSL)ordered
from1950to2017(seeS1Tableforalistofreviewedstudies).(B)Botanicalcollections(BC)from1857to2016(seeS2Tableforalistofherbariawhererecordsare
available).Thedotsrepresentthecumulativenumberofspecies,thesolidredlineistheresultofrandominterpolationofthesepoints,andthedashedredlineisthe
predictednumberofrecordedspecieswithincreasedeffort[48].Thegrayareadenotesthe95%confidenceintervaloftheestimatedcurves.
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ThetreespeciespoolofAmazonianwetlands
mostcomprehensiveestimatetodateoftheAmazoniantreespeciespoolthatcansurvive
underextremehydrologicalconditions.AlthoughthesamplingeffortdevotedtoAmazonian
uplandforestsiscurrentlyfourtimeshigherthantowetlandforests[11,23],ourtreespecies
listrepresents53%ofallthe6727treespeciesconfirmedfortheentireAmazonregion[9].
Assumingthistobeanaccurateestimateofthetrueproportion,Amazonianwetlandscould
harborc.a.8500ofthe16000treespeciesexpectedtocomprisethetotalAmazoniantreeflora
[11].
Mostlikely,othertreespeciesreportedfortheAmazonmayalsooccurinhydromorphic
environments,buthavenotyetbeenrecordedinAmazonianwetlands.Forinstance,theaver-
agecollectiondensityrecoveredbyus(TSL+BC)is0.020recordsper100km2ofAmazonian
wetlands,whenconsideringthe2.1millionkm2estimateof[20],or0.050recordsper100km2
ifconsideringthemorerestrictive840000km2mappedby[18].Thesesamplingdensitiesare
threeordersofmagnitudelowerthantheobserveddensityof10recordsper100km2forAma-
zonianforestsingeneral[9,51].Forthisreason,wealsoexpectthatanimportantportionof
treespeciesoccurringinAmazonianwetlandsmaynotbeyetknowntoscience.Forexample,
fromthe173treespeciesdiscoveredintheAmazonduringthefirstdecadeofthe21stcentury
[52],only21(12%)wereidentifiedinourestimatedspeciespool,andofthese,onlysixholo-
typespecimensseemtocomefromvoucherscollectedinAmazonianwetlandhabitats.We
thusemphasizethedireneedformoreintensiveandcomprehensivesamplingoftheAmazo-
nianwetlandenvironments.
Asecondlimitationofthepresentlistisintroducedbythebiastowardsspecificwetland
typeswithintheAmazon.BiodiversityassessmentsintheAmazonandelsewherearegenerally
biasedtowardsmajorurbancentersandalongmajorriversorroadways[9,53],andthisbiasis
showntowardsinventoriesofcertaintypesoffloodplainforests.Thecoverageofwetlandhabi-
tattypesandspeciesoccurrencesrecordedinourTSLandBCdatasetsshow,aspreviouslyrec-
ognizedby[23],thateutrophicfloodplainforests(várzeas)alonglarge“white-water”riversare
themostsampledwetlandforesttypeacrosstheAmazon.MostoftheAmazonianhumanpop-
ulationandmajorurbancentersareadjacenttotheseareas,andwefoundthelargestdensities
ofbotanicalrecordsalongtheAmazonasandNegrorivermainstems,nearmajorurbancen-
terswithwell-establishedresearchinstitutions(e.g.:Bele´m,Manaus,Tefe´,Iquitos).Amuch
lowerrecorddensitywasobservedalongthefloodplainwetlandsofothermajorAmazon
tributaries(e.g.:Putumayo-Ic¸a´;Jurua´;PurusandMadeira),orinriparianforestsalonginterflu-
vialareasoftheAmazonlowlands.
Athirdlimitationisthatwecouldnotuseoneineveryfour(25%)publishedtreesurveys
conductedinAmazonianwetlandforests,astheauthorsdidnotincludeexplicitandcomplete
specieslistsinthepublications.Althoughthe21stcenturyhasseentheriseofcollaborativenet-
works,andcomprehensivechecklistsforNeotropicalforestsprovidelargeamountsofvaluable
information,westillneedadeeperculturalshiftamongresearchers,favoringdatasharingand
transparency,ifwearetoimproveourcombinedknowledgeoftropicaltreebiodiversity[54].
Itissurprisingthatthetwodatasetsweinvestigatedsharedlessthanhalfofthetotalnumberof
validtreespeciesrecorded,aswewouldexpectcompleteoverlapunderanidealscenario
whereatleastonevoucherspecimenwasdepositedforeachspeciesrecordedineachreviewed
inventory(withvouchersproperlydigitizedandmadeavailableonlineinherbariadatabases).
However,althoughmostpublishedinventorystudiesclaimedtohavedepositedvoucherspeci-
mensfortheirsampledplots,wewereunabletofindnearlyathirdofthespeciesreportedfor
inventoryplotsinthedigitizedherbariasources.Veryoften,easilyrecognizablespeciesand
specimenswithoutfertilestructuresarenotincludedinvouchercollections,creatinga“data
void”intheherbariarecords[51].Thus,inpractice,inventoriesandisolatedbotanicalcollec-
tionsprovidecomplementaryfloristicinformationforassessingtreespeciesdiversity.This
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ThetreespeciespoolofAmazonianwetlands
reinforcestheneedforincludingthecompletespecieslistsinpublishedinventoriesandshows
thatscientistsneedtokeepperformingbothtypesofstudiesifwearetoincreaseourknowl-
edgeoftheAmazonwetlandtreediversity.
Finally,amorecomprehensiveknowledgeoftheAmazonwetlandstreespeciespoolcanbe
achievedthrougheffortsinreducingotherbiologicalshortfalls(sensu[55]).Forinstance,the
uncertaintyregardingactuallife-form(i.e.:tree)oftherecordedplantspecies(“Raunkiaeran
shortfall”),andthelackofvoucherdeterminationsandtaxonomicreviewsformostherbaria
records(“Linneanshortfall”),resultedintheremovalofc.a.25000recordsand6000species
namesoriginallypresentintheBCdatasetaftertaxonomicstandardizationandmatchingto
thetreespecieslistof[9].Furthermore,manysamplesdidnotincludeinformationonhabitat
conditions,precludingadetailedassessmentofspeciesoccurrencebywetlandtype(e.g.:vár-
zea,igapó,campinas,tidalvárzeas).Moreeffortsshouldbemadetoensureforthcomingbotan-
icalcollectionsandinventoriesexplicitlyincludelifeformandspecifichabitatconditions,as
wellasotherecologicallyrelevantinformation.
HowdoestheAmazonianwetlandspeciespoolcomparetothebasin-wide
speciespool?
ThetreespeciespoolofAmazonwetlandscomprised104botanicalfamiliesdistributedinto
689genera,withelevenfamilieshavingmorethan100treespecieseach.Leguminosae(578
treespecies),Rubiaceae(220treespecies),Annonaceae(182treespecies),Lauraceae(175tree
species),andMyrtaceae(155treespecies)werethemostdiversetreefamiliesinAmazonian
wetlandforests,comprisingtogether36%oftheAmazonianwetlandstreespeciespool.The
tenrichestfamiliesinAmazonianwetlandsaccountedfor53%oftheentirespeciespool
(Table1).
Although69treefamilieshadhalformoreoftheirAmazoniantaxaoccurringinAmazon
wetlands,includingsomeoftherichestwetlandfamilies(Leguminosae,Euphorbiaceaeand
Moraceae,Table1),wedidnotfindanywetlandrecordsfor15familieswithknownoccur-
renceinAmazonforests.Overall,c.a.51%oftheAmazoniantreespecieswithineachfamily
occurredinwetlandhabitats,buttherewerenoticeabledifferencesinrankorderandpercent-
ageofsharedspeciesbetweenthetenrichestwetland-occurringfamiliesandtheirrespective
richnessrankingwithintheoverallAmazonflora,asgivenby[9](Table1).
Table1. TreespeciesrichnessforthetenrichestbotanicalfamiliesfoundinAmazonianwetlandscomparedwiththeirrichnessrankingaccordingtotheAmazon
treeflora.
Family Richnessrankingfor 1Richnessrankingfor Numberofvalidtree Numberofvalidtree Percentofspecies
Amazonianwetlandstree Amazoniantreeflora speciesinAmazon speciesinentireAmazon occurringinwetlands
speciespool Wetlands flora1 (%)
Leguminosae 1 1 578 1042 55
Rubiaceae 2 5 220 338 65
Annonaceae 3 4 182 388 46
Lauraceae 4 2 175 400 43
Myrtaceae 5 3 155 393 39
Melastomataceae 6 6 136 263 51
Chrysobalanaceae 7 7 132 256 51
Sapotaceae 8 8 128 244 52
Euphorbiaceae 9 11 114 160 71
Moraceae 10 13 112 147 76
1Following[9].
https://doi.org/10.1371/journal.pone.0198130.t001
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ThetreespeciespoolofAmazonianwetlands
Fig3.Per-genusproportionofAmazoniantreespeciesoccurringandnotoccurringinwetlands.Proportionsarecalculatedforthe803generalistedtheAmazon
treespecieschecklist[9]andrankedfromhighertolowerproportionofspeciesonwetlands.
https://doi.org/10.1371/journal.pone.0198130.g003
Atthegenuslevel,221generaintheAmazontreechecklist[9]hadallitsknownspecies
recordedintheAmazonwetlandstreespeciespool(Fig3).However,manyofthesegenera
(124)hadonlyasingleacceptedspeciesoccurringintheAmazon,withonlyeightgenerahav-
ing10ormoreknownspecies(max.26species).Conversely,201generalistedontheAmazon
treechecklist[9]hadnospeciesrecordedinAmazonianwetlands(Fig3).Therichestgenusin
AmazonwetlandsisInga(85treespecies),followedbyLicania(69species),Miconia(69spe-
cies),Pouteria(69species),andEugenia(59species).
TheecologicalandevolutionaryroleofAmazonianwetlands
ThefilteredtreespeciespoolforAmazonianwetlandforestsincludesalmostallbotanicalfami-
liesknowntooccurinAmazonforests.Itiscomparabletothe3389treespeciesacknowledged
fortheentireBrazilianAtlanticForest[56],oneofthemostbiodiverseNeotropicalbiomes.
Onepossibleexplanationforthisrichnessisthat,asAmazonianuplandandwetlandareasare
contiguoushabitatsknowntohaveaninterchangeableflora[34,40],wecanexpectahigh
degreeoflateralmigrationsamongthesehabitats,withalargeproportionoftreespeciesin
eachlineagereachingandeventuallyadaptingtobothfloodedandnon-floodedforestedhabi-
tats.Still,differentpatternsmightalsobeplausible.Forinstance,thecontributionoftreespe-
ciesoccurringinAmazonianwetlandstothetotaldiversityoftheAmazon-centeredgenus
suggestsometaxahaveevolvedahighdegreeofinsituspecializationonwetlands,onlythen
colonizinguplandhabitats.Despitethehighlikelihoodthatatreespecieswillreachwetland
habitatswhenmigratingacrosstheAmazonlandscape,manyAmazoniantreespeciesdonot
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ThetreespeciespoolofAmazonianwetlands
showpreferenceforfloodedhabitats;c.a.64%ofthe4963treespeciesrecordedinATDN
database[11],withonly68ofthe600mostcommontreespeciesoccurringinwhite-water
Amazonfloodplainforestseemingtobehabitatendemics[34].Assessingphylogenetichistory
andtherelativecontributionofeachdirectionofmigrationtodiversificationcouldgiveus
importantinsightontheoriginandevolutionaryhistoryofseveralimportanttaxaintheAma-
zontreeflora,andtheroleofstrongenvironmentalfilteringandhydrologicalnichespecializa-
tioninthisprocess,ashasbeenshownforBrazilianCerradospeciesinrelationtofire
disturbance[57].
Growingevidencesuggeststhatitisreasonabletothinkofatreespeciespoolcomprisedby
theentireAmazonregion[13],buttheroleofecologicalfilteringintheassemblyoflocalcom-
munitiescannotbeexcluded[58].ThecontinentaldimensionsoftheAmazonbiomeandthe
virtuallackofgeographicbarriersforplantspeciesacrossthelowlandsimpliesfewdispersal
limitationsfortreespecies[13].Newenvironmentalconditionsarereachedwhenspecies
expandtheirdistributions,andthisfloristicinterchangebetweenwetlandanduplandhabitats
mightmodulatesource-sinkpopulationdynamicsacrossmarginalhabitats.Atecologicaltime-
scales,source-sinkdynamicswillaffectpopulationregulationandspeciescoexistence[59,60];
overevolutionarytimescales,itwillselectecotypesmorepronetocolonizecertainhabitats,
leadingtogeneticandmorphologicaldifferentiationamongpopulations[30,58,61].Inthis
context,althoughtheAmazonianhydrologicalgradientsaremoreidiosyncraticthanthecon-
spicuousandwidelydiscussedtemperaturegradientsalongAndeanmountainslopes,thereis
ampleevidenceforselectivepressuresactingonthehydrologicalnichedimensionofAmazo-
niantreespecies,stronglyaffectingvegetationdevelopmentandthedistributionofspecies
diversityacrosstheregion[11,39,62].Therefore,theselowlandhydrologicalgradientsare
verylikelytohavehadastronghistoricalroleontreespeciesdiversification,rangeexpansion
[34,38,42,63],andlocalcommunityassembly[37,39].
Conclusions
WeshowthatthetreespeciespoolofAmazonianwetlandscomprises53%(3615)ofthecon-
firmedtreespeciesoccurringintheoverallAmazon,raisingpreviousrichnessestimatesbya
factorof3.2.Itisverylikelythatmanyofthesespecieswillalsooccurinotherforestedhabitats,
orevenotherNeotropicalregions.AlargeportionoftheNeotropicalplantdiversityisencom-
passedbyAmazon-centeredtaxaandunderstandingtheirevolutionaryandecologicalhisto-
riescanimproveourknowledgeofthedevelopmentofthishyperdiversebiogeographicrealm.
GeographicalbarriersforplantdispersalaremostlyabsentintheAmazonregion,whichis
insteadcharacterizedbyamosaicofhabitattypesandenvironmentalgradients,includingwet-
landhabitatsthathavebeenpervasivelypresentsincebeforetheAndeanuplift.Furtherstudies
thatcandisassembleandthencontrasttheAmazontreefloraintothefilteredspeciespools
associatedwitheachhabitattypearenecessarytoopennewavenuesforexploringtheecologi-
calandgeographicdistributionofAmazoniantreespecies,functionaltypes,andlineages,and
unveiltherelativeroleofdispersalandenvironmentalfilteringoncommunityassemblyand
ontheoriginsandmaintenanceofspeciesdiversityovertime.
Supportinginformation
S1Table.Referencelistforreviewedtreespecieslists.
(XLSX)
S2Table.ListofherbariaavailableonSpeciesLinkthatcontributedwithrecords.
(XLSX)
PLOSONE|https://doi.org/10.1371/journal.pone.0198130 May29,2018 9/13
ThetreespeciespoolofAmazonianwetlands
S3Table.ChecklistoftheAmazonianwetlandstreespeciespool.
(XLSX)
Acknowledgments
WethankLuciaG.LohmannandAnaCarolinaC.Carnavalforhelpfuldiscussionswhenplan-
ningthescopeofthismanuscript.
AuthorContributions
Conceptualization:BrunoGarciaLuize,EduardoMartinsVenticinque,EvlynMa´rciaLeãode
MoraesNovo,ThiagoSannaFreireSilva.
Datacuration:BrunoGarciaLuize.
Formalanalysis:BrunoGarciaLuize,ThiagoSannaFreireSilva.
Fundingacquisition:HelderQueiroz,MariaAparecidaLopes,EduardoMartinsVenticinque,
EvlynMa´rciaLeãodeMoraesNovo,ThiagoSannaFreireSilva.
Investigation:BrunoGarciaLuize,Jose´LeonardoLimaMagalhães.
Methodology:BrunoGarciaLuize.
Projectadministration:HelderQueiroz,MariaAparecidaLopes,EduardoMartinsVenticin-
que,EvlynMa´rciaLeãodeMoraesNovo,ThiagoSannaFreireSilva.
Supervision:ThiagoSannaFreireSilva.
Validation:BrunoGarciaLuize.
Visualization:BrunoGarciaLuize,EduardoMartinsVenticinque,ThiagoSannaFreireSilva.
Writing–originaldraft:BrunoGarciaLuize,ThiagoSannaFreireSilva.
Writing–review&editing:BrunoGarciaLuize,Jose´LeonardoLimaMagalhães,Helder
Queiroz,MariaAparecidaLopes,EduardoMartinsVenticinque,EvlynMa´rciaLeãode
MoraesNovo,ThiagoSannaFreireSilva.
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